Gene expression profiling in the early phases of DMD: A constant molecular signature characterizes DMD muscle from early postnatal life throughout disease progression

FASEB Journal

Volumn 21, Issue 4, 2007, Pages 1210-1226

  Pescatori, Mario ^a,f   Broccolini, Aldobrando ^a   Minetti, Carlo ^b   Bertini, Enrico ^c   Bruno, Claudio ^b   D'Amico, Adele ^c   Bernardini, Camilla ^a   Mirabella, Massimiliano ^a,f   Silvestri, Gabriella ^a   Giglio, Vincenzo ^d,e   Modoni, Anna ^a   Pedemonte, Marina ^b   Tasca, Giorgio ^a   Galluzzi, Giuliana ^e   Mercuri, Eugenio ^a   Tonali, Pietro A ^a,f   Ricci, Enzo ^a,f  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^d SAN PAOLO HOSPITAL   (Italy)

^e UILDM   (Italy)

^f IRCCS FONDAZIONE DON CARLO GNOCCHI   (Italy)

Author keywords

Duchenne muscular dystrophy; Human disease; Microarrays; Wnt, Notch, and BMP signaling

Indexed keywords

NOTCH RECEPTOR; PROCOLLAGEN C PROTEINASE; WNT PROTEIN;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DUCHENNE MUSCULAR DYSTROPHY; ENERGY METABOLISM; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INFLAMMATION; MOLECULAR BIOLOGY; PATHOPHYSIOLOGY; POSTNATAL GROWTH; PRIORITY JOURNAL;

AGE FACTORS; ANIMALS; CHILD, PRESCHOOL; DISEASE PROGRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; GENOME; HUMANS; INFANT; INFLAMMATION; MICE; MUSCLES; MUSCULAR DYSTROPHY, DUCHENNE; TIME FACTORS;

EID: 33947655852     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7285com     Document Type: Article

References (76)

1. Hoffman, E. P., Brown, R. H., Jr., and Kunkel, L. M. (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51, 919-928
2. Straub, V., and Campbell, K. P. (1997) Muscular Dystrophies and the dystrophin-glycoprotein complex. Curr. Opin. Neurol. 10, 168-175 (review)
3. Chen, Y-W., Zhao, P., Borup, R., and Hoffman, E. P. (2000) Expression profiling in the muscular dystrophies: identification of novel aspects of molecular pathophysiology. J. Cell Biol. 151, 1321-1336
4. Haslett, J. N., Sanoudou, D., Kho, A. T., Bennett, R. R., Greenberg, S., Kohane, I. S., Beggs, A. H., and Kunkel, L. M. (2002) Gene expression comparison of biopsies from Duchenne muscular dystrophy (DMD) and normal skeletal muscle. Proc. Natl. Acad. Sci. U. S. A. 99, 15000-15005
5. Bakay, M., Zhao, P., Chen, J., and Hoffman, E. P. (2002) A web-accessible complete transcriptome of normal human and DMD muscle. Neuromuscul. Disord. Suppl. 1, S125-S141
6. Bakay, M., Chen, Y. W., Borup, R., Zhao, P., Nagaraju, K., and Hoffman, E. P. (2002) Sources of variability and effect of experimental approach on expression profiling data interpretation. BMC Bioinformatics 3, 4
7. Haslett, J. N., Sanoudou, D., Kho, A. T., Han, M., Bennett, R. R., Kohane, I. S., Beggs, A., and Kunkel, L. M. (2003) Gene expression profiling of Duchenne muscular dystrophy skeletal muscle. Neurogenetics 4, 163-171
8. Simon, R., Korn, E., McShane, L., Radmacher, M., Wright, G., and Zhao, Y. (2003) Design and Analysis of DNA Microarray Investigations, Springer-Verlag, New York
9. Korn, E. L., Troenndle, J. F., McShane, L. M., and Simon, R. (2003) Controlling the number of false discoveries: Application to high-dimensional genomic data. J. Stat. Plan. Inference 124, 2448-2455
10. Simon, R., and Lam, A. BRB-ArrayTools User Guide, version 3.2. Biometric Research Branch, National Cancer Institute, NIH. http://linus.nci.nih. gov/brb
11. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B., and Speed, T. P. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15
12. Pavlidis, P., Weston, J., Cai, J., and Noble, W. S. (2002) Learning gene functional classifications from multiple data types. J. Comput. Biol. 9, 401-411
13. Pizon, V., Gerbal, F., Diaz, C. C., and Karsenti, E. (2005) Microtubule-dependent transport and organization of sarcomeric myosin during skeletal muscle differentiation. EMBO J. 24, 3781-3792
14. Mishina, M., Takai, T., Imoto, K., Noda, M., Takahashi, T., Numa, S., Methfessel, C., and Sakmann, B. (1986) Molecular distinction between fetal and adult forms of muscle acetylcholine receptor. Nature 321, 406-411
15. Gu, Y., and Hall, Z. W. (1988) Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle. Neuron 1, 117-125
16. Chelly, J., Gilgenkrantz, H., Lambert, M., Hamard, G., Chafey, P., Recan, D., Katz, P., de la Chapelle, A., Koenig, M., Ginjaar, I. B., et al. (1990) Effect of dystrophin gene deletions on mRNA levels and processing in Duchenne and Becker muscular dystrophies. Cell 63, 1239-1248
17. Grounds, M. D. (1991) Towards understanding skeletal muscle regeneration. Pathol. Res. Pract. 187, 1-22
18. Weintraub, H. (1993) The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75, 1241-1244
19. Lee, S. J. (2004) Regulation of muscle mass by myostatin. Annu. Rev. Cell Dev. Biol. 20, 61-86
20. Schuelke, M., Wagner, K. R., Stolz, L. E., Hubner, C., Riebel, T., Komen, W., Braun, T., Tobin, J. F., and Lee, S. J. (2004) Myostatin mutation associated with gross muscle hypertrophy in a child. N. Engl. J. Med. 350, 2682-2688
21. Jackman, R. W., and Kandarian, S. C. (2004) The molecular basis of skeletal muscle atrophy. Am. J. Physiol. 287, C834-C843
22. Winn, N., Paul, A., Musaro, A., and Rosenthal, N. (2002) Insulin-like growth factor isoforms in skeletal muscle aging, regeneration, and disease. Cold Spring Harb. Symp. Quant. Biol. 67, 507-518
23. Broccolini, A., Ricci, E., Pescatori, M., Papacci, M., Gliubizzi, C., D'Amico, A., Servidei, S., Tonali, P., and Mirabella, M. (2004) Insulin-like growth factor I in inclusion-body myositis and human muscle cultures. J. Neuropathol. Exp. Neurol. 63, 650-659
24. Musaro, A., Giacinti, C., Borsellino, G., Dobrowolny, G., Pelosi, L., Cairns, L., Ottolenghi, S., Cossu, G., Bernardi, G., Battistini, L., et al. (2004) Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc. Natl. Acad. Sci. U. S. A. 101, 1206-1210
25. Barton, E. R., Morris, L., Musaro, A., Rosenthal, N., and Sweeney, H. L. (2002) Muscle-specific expression of insulin-like growth factor I counters muscle decline in mdx mice. J. Cell Biol. 157, 137-148
26. Engvall, E., and Wewer, U. M. (2003) The new frontier in muscular dystrophy research: booster genes. FASEB J. 17, 1579-1584
27. Zumbrunn, J., and Trueb, B. (1996) Primary structure of a putative serine protease specific for IGF-binding proteins. FEBS Lett. 398, 187-192
28. Kominami, E., Kunio, I., and Katunuma, N. (1987) Activation of the intramyofibral autophagic-lysosomal system in muscular dystrophy. Am. J. Pathol. 127, 461-466
29. Spencer, M. J., and Mellgren, R. L. (2002) Overexpression of a calpastatin transgene in mdx muscle reduces dystrophic pathology. Hum. Mol. Genet. 11, 2645-2655
30. Tidball, J. G., and Spencer, M. J. (2000) Calpains and muscular dystrophies. Int. J. Biochem. Cell Biol. 32, 1-5
31. Combaret, L., Taillandier, D., Voisin, L., Samuels, S. E., Boespflug-Tanguy, O., and Attaix, D. (1996) No alteration in gene expression of components of the ubiquitin-proteasome proteolytic pathway in dystrophin-deficient muscles. FEBS Lett. 393, 292-296
32. Bonuccelli, G., Sotgia, F., Schubert, W., Park, D. S., Frank, P. G., Woodman, S. E., Insabato, L., Cammer, M., Minetti, C., and Lisanti, M. P. (2003) Proteasome inhibitor (MG-132) treatment of mdx mice rescues the expression and membrane localization of dystrophin and dystrophin-associated proteins. Am. J. Pathol. 163, 1663-1675
33. Shurin, G. V., Ferris, R. L., Tourkova, I. L., Perez, L., Lokshin, A., Balkir, L., Collins, B., Chatta, G. S., and Shurin, M. R. (2005) Loss of new chemokine CXCL14 in tumor tissue is associated with low infiltration by dendritic cells (DC), while restoration of human CXCL14 expression in tumor cells causes attraction of DC both in vitro and in vivo. J. Immunol. 174, 5490-5498
34. Chen, Y. W., Nagaraju, K., Bakay, M., McIntyre, O., Rawat, R., Shi, R., and Hoffman, E. P. (2005) Early onset of inflammation and later involvement of TGFbeta in Duchenne muscular dystrophy. Neurology 65, 826-834
35. Messina, S., Bitto, A., Aguennouz, M., Minutoli, L., Monici, M. C., Altavilla, D., Squadrito, F., and Vita, G. (2006) Nuclear factor kappa-B blockade reduces skeletal muscle degeneration and enhances muscle function in Mdx mice. Exp. Neurol. 198, 234-241
36. Messina, S., Altavilla, D., Aguennouz, M., Seminara, P., Minutoli, L., Monici, M. C., Bitto, A., Mazzeo, A., Marini, H., Squadrito, F., and Vita, G. (2006) Lipid peroxidation inhibition blunts nuclear factor-kappaB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am. J. Pathol. 168, 918-926
37. Stamenkovic, I. (2003) Extracellular matrix remodelling: the role of matrix metalloproteinases. J. Pathol. 200, 448-464 (review)
38. Von Moers, A., Zwirner, A., Reinhold, A., Bruckmann, O., van Landeghem, F., Stoltenburg-Didinger, G., Schuppan, D., Herbst, H., and Schuelke, M. (2005) Increased mRNA expression of tissue inhibitors of metalloproteinase-1 and -2 in Duchenne muscular dystrophy. Acta Neuropathol. (Berlin) 109, 285-293
39. Arthur, M. J., Iredale, J. P., and Mann, D. A. (1999) Tissue inhibitors of metalloproteinases: role in liver fibrosis and alcoholic liver disease. Alcohol. Clin. Exp. Res. 23, 940-943 (review)
40. Gueders, M. M., Foidart, J. M., Noel, A., and Cataldo, D. D. (2006) Matrix metalloproteinases (MMPs) and tissue inhibitors of MMPs in the respiratory tract: potential implications in asthma and other lung diseases. Eur. J. Pharmacol. 533, 133-144 (review)
41. Leask, A., and Abraham, D. J. (2004) TGF-beta signalling and the fibrotic response. FASEB J. 18, 816-827 (review)
42. Yamazaki, M., Minota, S., Sakurai, H., Miyazono, K., Yamada, A., Kanazawa, I., and Kawai, M. (1994) Expression of transforming growth factor-beta 1 and its relation to endomysial fibrosis in progressive muscular dystrophy. Am. J. Pathol. 144, 221-226
43. Lundberg, I., Brengman, J. M., and Engel, A. G. (1995) Analysis of cytokine expression in muscle in inflammatory myopathies, Duchenne dystrophy, and non-weak controls. J. Neuroimmunol. 63, 9-16
44. Bernasconi, P., Torchiana, E., Confalonieri, P., Brugnoni, R., Barresi, R., Mora, M., Cornelio, F., Morandi, L., and Mantegazza, R. (1995) Expression of transforming growth factor-beta 1 in dystrophic patient muscles correlates with fibrosis. Pathogenetic role of a fibrogenic cytokine. J. Clin. Invest. 96, 1137-1144
45. Gosselin, L. E., Williams, J. E., Deering, M., Brazeau, D., Koury, S., and Martinez, D. A. (2004) Localization and early time course of TGF-beta 1 mRNA expression in dystrophic muscle. Muscle Nerve 30, 645-653
46. Zhou, L., Porter, J. D., Cheng, G., Gong, B., Hatala, D. A., Merriam, A. P., Zhou, X., Rafael, J. A., and Kaminski, H. J. (2006) Temporal and spatial mRNA expression patterns of TGF-beta1, 2, 3 and TbetaRI, II, III in skeletal muscles of mdx mice. Neuromuscul. Disord. 16, 32-38
47. Okamoto, O., Fujiwara, S., Abe, M., and Sato, Y. (1999) Dermatopontin interacts with transforming growth factor beta and enhances its biological activity. Biochem. J. 337, 537-541
48. Zanotti, S., Negri, T., Cappelletti, C., Bernasconi, P., Canioni, E., Di Blasi, C., Pegoraro, E., Angelini, C., Ciscato, P., Prelle, A., Mantegazza, R., et al. (2005) Decorin and biglycan expression is differentially altered in several muscular dystrophies. Brain 128, 2546-2555
49. Nishio, H., Wada, H., Matsuo, T., Horikawa, H., Takahashi, K., Nakajima, T, Matsuo, M., and Nakamura, H. (1990) Glucose, free fatty acid and ketone body metabolism in Duchenne muscular dystrophy. Brain Dev. 12, 390-402
50. Honke, K., Hasui, M., and Takano, N. (1997) Abnormal metabolism of fatty acids and ketone bodies in Duchenne muscular dystrophy, and the effect of biotin on these abnormalities No To Hattatsu 29, 13-18 (Japanese)
51. Polesskaya, A., Seale, P., and Rudnicki, M. A. (2003) Wnt signalling induces the myogenic specification of resident CD45+ adult stem cells during muscle regeneration. Cell 113, 841-852
52. Seale, P., Polesskaya, A., and Rudnicki, M. A. (2003) Adult stem cell specification by Wnt signalling in muscle regeneration. Cell Cycle 2, 418-419 (review)
53. Torrente, Y., Belicchi, M., Sampaolesi, M., Pisati, F., Meregalli, M., D'Antona, G., Tonlorenzi, R., Porretti, L., Gavina, M., Mamchaoui, K., et al. (2004) Human circulating AC133(+) stem cells restore dystrophin expression and ameliorate function in dystrophic skeletal muscle. J. Clin. Invest. 114, 182-195
54. Tagliafico, E., Brunelli, S., Bergamaschi, A., De Angelis, L., Scardigli, R., Galli, D., Battini, R., Bianco, P., Ferrari, S., Cossu, G., and Ferrari, S. (2004) TGFbeta/BMP activate the smooth muscle/bone differentiation programs in mesoangioblasts. J. Cell Sci. 117, 4377-4388
55. Garces, C., Ruiz-Hidalgo, M. J., Bonvini, E., Goldstein, J., and Laborda, J. (1999) Adipocyte differentiation is modulated by secreted delta-like (dlk) variants and requires the expression of membrane-associated dlk. Differentiation 64, 103-114
56. Smas, C. M., Chen, L., and Sul, H. S. (1997) Cleavage of membrane-associated pref-1 generates a soluble inhibitor of adipocyte differentiation. Mol. Cell. Biol. 17, 977-988
57. Davis, E., Jensen, C. H., Schroder, H. D., Farnir, F., Shay-Hadfield, T., Kliem, A., Cockett, N., Georges, M., and Charlier, C. (2004) Ectopic expression of DLK1 protein in skeletal muscle of padumnal heterozygotes causes the callipyge phenotype. Curr. Biol. 14, 1858-1862
58. Balemans, W., and Van Hul, W. (2002) Extracellular regulation of BMP signalling in vertebrates: a cocktail of modulators. Dev. Biol. 250, 231-250 (review)
59. Katoh, M., and Katoh, M. (2006) CER1 is a common target of WNT and NODAL signalling pathways in human embryonic stem cells. Int. J. Mol. Med. 17, 795-799
60. Musgrave, D. S., Pruchnic, R., Wright, V., Bosch, P., Ghivizzani, S. C., Robbins, P. D., and Huard, J. (2001) The effect of bone morphogenetic protein-2 expression on the early fate of skeletal muscle-derived cells. Bone 28, 499-506
61. Dahlqvist, C., Blokzijl, A., Chapman, G., Falk, A., Dannaeus, K., Ibanez, C. F., and Lendahl, U. (2003) Functional Notch signalling is required for BMP4-induced inhibition of myogenic differentiation. Development 130, 6089-6099
62. Porter, J. D., Merriam, A. P., Leahy, P., Gong, B., and Khanna, S. (2003) Dissection of temporal gene expression signatures of affected and spared muscle groups in dystrophin-deficient (mdx) mice. Hum. Mol. Genet. 12, 1813-1821
63. Porter, J. D., Merriam, A. P., Leahy, P., Gong, B., Feuerman, J., Cheng, G., and Khanna, S. (2004) Temporal gene expression profiling of dystrophin-deficient (mdx) mouse diaphragm identifies conserved and muscle group-specific mechanisms in the pathogenesis of muscular dystrophy Hum. Mol. Genet. 13, 257-269
64. Porter, J. D., Khanna, S., Kaminski, H. J., Rao, J. S., Merriam, A. P., Richmonds, C. R., Leahy, P., Li, J., Guo, W., and Andrade, F. H. (2002) A chronic inflammatory response dominates the skeletal muscle molecular signature in dystrophin-deficient mdx mice. Hum. Mol. Genet. 11, 263-272
65. Greenberg, S. A., Sanoudou, D., Haslett, J. N., Kohane, I. S., Kunkel, L. M., Beggs, A. H., and Amato, A. A. (2002) Molecular profiles of inflammatory myopathies. Neurology 59, 1170-1182
66. Tezak, Z., Hoffman, E. P., Lutz, J. L., Fedczyna, T. O., Stephan, D., Bremer, E. G., Krasnoselska-Riz, I., Kumar, A., and Pachman, L. M. (2002) Gene expression profiling in DQA1*0501+ children with untreated dermatomyositis: a novel model of pathogenesis. J. Immunol. 168, 4154-4163
67. Yan, Z., Choi, S., Liu, X., Zhang, M., Schageman, J. J., Lee, S. Y., Hart, R., Lin, L., Thurmond, F. A., and Williams, R. S. (2003) Highly coordinated gene regulation in mouse skeletal muscle regeneration. J. Biol. Chem. 278, 8826-8836
68. Paoni, N. F., Peale, F., Wang, F., Errett-Baroncini, C., Steinmetz, H., Toy, K., Bai, W., Williams, P. M., Bunting, S., Gerritsen, M. E., and Powell-Braxton, L. (2002) Time course of skeletal muscle repair and gene expression following acute hind limb ischemia in mice. Physiol. Genomics 11, 263-272
69. Goetsch, S. C., Hawke, T. J., Gallardo, T. D., Richardson, J. A., and Garry, D. J. (2003) Transcriptional profiling and regulation of the extracellular matrix during muscle regeneration. Physiol. Genomics 14, 261-271
70. Matecki, S., Guibinga, G. H., and Petrof, B. J. (2004) Regenerative capacity of the dystrophic (mdx) diaphragm after induced injury. Am. J. Physiol. 287, R961-R968
71. Oexle, K., and Kohlschutter, A. (2001) Cause of progression in Duchenne muscular dystrophy: impaired differentiation more probable than replicative aging. Neuropediatrics 32, 123-129
72. Conboy, I. M., Conboy, M. J., Smythe, G. M., and Rando, T. A. (2003) Notch-mediated restoration of regenerative potential to aged muscle. Science 302, 1575-1577
73. Conboy, I. M., Conboy, M. J., Wagers, A. J., Girma, E. R., Weissman, I. L., and Rando, T. A. (2005) Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 433, 760-764
74. Muntoni, F., Fisher, I., Morgan, J. E., and Abraham, D. (2002) Steroids in Duchenne muscular dystrophy: from clinical trials to genomic research. Neuromuscul. Disord. 12, S162-S165
75. 't Hoen P. A., van der Wees C. G., Aartsma-Rus A., Turk R., Goyenvalle A., Danos O., Garcia L., van Ommen G. J., den Dunnen J. T., and van Deutekom J. C. (2006) Gene expression profiling to monitor therapeutic and adverse effects of antisense therapies for Duchenne muscular dystrophy. Pharmacogenomics 7, 281-297
76. Balagopal, P., Olney, R., Darmaun, D., Mougey, E., Dokler, M., Sieck, G., and Hammond, D. (2006) Oxandrolone enhances skeletal muscle myosin synthesis and alters global gene expression profile in Duchenne muscular dystrophy. Am. J. Physiol. 290, E530-E539